REVIEW

Neosomes of tungid fleas on wild and domestic animals

Pedro Marcos Linardi & Daniel Moreira de Avelar

Received: 2 June 2014 /Accepted: 11 August 2014 /Published online: 21 August 2014# The Author(s) 2014. This article is published with open access at Springerlink.com

Abstract Tunga is the most specialized genus among theSiphonaptera because adult females penetrate into the skinof their hosts and, after mating and fertilization, undergohypertrophy, forming an enlarged structure known as theneosome. In humans and other warm-blooded animals,neosomes cause tungiasis, which arises due to the action ofopportunistic agents. Although its effects on humans anddomestic animals are well described in the literature, little isknown about the impact of tungiasis on wild animals. Thisreview focuses on the morphology, taxonomy, geographicaldistribution, hosts, prevalence, sites of attachment, and impactof tungid neosomes on wild and domestic animals. Becauseneosomes are the most characteristic form of the genus Tungaand also the formmost frequently found in hosts, they are heredifferentiated and illustrated to aid in the identification of the13 currently known species. Perspectives for future studiesregarding the possibility of discovering other sand flea spe-cies, adaptation to new hosts, and the transfer of tungidsbetween hosts in natural and modified habitats are alsopresented.

Keywords Neosome . Tungid fleas . Sand fleas .Wild anddomestic animals . Siphonaptera

Introduction

Adult fleas (Siphonaptera) are obligate hematophagousectoparasites that infest humans and wild and domesticanimals. There are approximately 3,000 species and sub-species of fleas included in 238 genera and 15 familiesworldwide (Lewis 1998). Tungidae is the most specializedfamily in that the females of the genera Tunga Jarocki(Tunginae) penetrate the skin of their hosts (Hopkins andRothschild 1953; Linardi and Guimarães 2000), and aftermating, the gravid females undergo hypertrophy, becomingneosomes (Audy et al. 1972) in spite of the genusNeotunga Smit of the family Pulicidae also present pene-trating females. Another genus, Hectopsylla Frauenfeld(Hectopsyllinae), includes species that are also consideredneosomatic, but the females are semipenetrating and onlyattach their mouthparts to the hosts.

According to Audy et al. (1972), neosomes are organismsthat are altered by the formation of a new external morpho-logical structure and the secretion of new cuticle, accompa-nied by significant enlargement during an active process ofmetamorphosis. Although neosomy exists in otherArthropoda, in fleas, the process occurs in approximately 90sessile or semisessile species (Rothschild 1992), primarily inthe families Vermipsyllidae and Tungidae. Neosomaticvermipsyllids, also called alakurt fleas, include two spe-cies—Dorcadia ioffi Smit and Vermipsylla alakurtSchimkewitsch—that parasitize ungulates, particularly do-mestic sheep, horses, and yaks in Central Asia, but theirfemales do not burrow beneath the skin as do tungids, whichare endoparasitic.

In tungids, neosomes are the most frequently observedform in hosts. Because neosomes involute with the death ofthe parasite after oviposition (Lavoipierre et al. 1979), specificidentification can be difficult because certain characteristicscannot be observed in the most commonly dissected

Electronic supplementary material The online version of this article(doi:10.1007/s00436-014-4081-8) contains supplementary material,which is available to authorized users.

P. M. Linardi (*)Departamento de Parasitologia, Instituto de Ciências Biológicas daUniversidade Federal de Minas Gerais, Caixa Postal 486, AvenidaAntônio Carlos, 6627, Campus UFMG, Belo Horizonte, MinasGerais 31270-901, Brazile-mail: linardi@icb.ufmg.br

D. M. de AvelarLaboratório de Pesquisas Clínicas, Centro de Pesquisas RenéRachou, Fundação Oswaldo Cruz, Belo Horizonte, Minas Gerais,Brazil

Parasitol Res (2014) 113:3517–3533DOI 10.1007/s00436-014-4081-8

specimens. Later, the neosomes can be absorbed or sloughedfrom the host epidermis by tissue repair mechanisms (Eiseleet al. 2003; Lavoipierre et al. 1979).

Whereas Neotunga is composed of only one valid species,Neotunga euloidea Smit, which parasitizes African pangolins(Lewis 1998), the genus Tunga includes 13 species of sandfleas (De Avelar et al. 2013). Two Tunga species are found inChina and Japan, and the other 11 occur in the New Worldtropics. One of these, Tunga penetrans (L., 1758), also occursin Sub-Saharan Africa (Beaucournu et al. 2012b; De Avelaret al. 2012; Lewis 1998; Linardi and Guimarães 2000).

However, because there is little knowledge of this group,some misidentifications have been recorded, especially giventhat many specimens collected from parasitological investiga-tions or veterinary surveys were named according to theirhosts. This circumstance is compounded by the fact that, withthe exception of De Avelar et al. (2012), taxonomic keysrarely contain data on neosomes.

Tungiasis causes serious ectoparasitosis, and harmfulinfections and their effects on humans are well documented,especially in Heukelbach (2005, 2006) and Karunamoorthi(2013). With respect to domestic animals, a review can befound in Pampiglione et al. (2009). However, little is knownabout the impact of tungiasis on wild animals. The presentarticle provides a selective review of the morphology, taxon-omy, geographical distribution, hosts, prevalence, preferredsites of attachment, and impact of neosomes on wild anddomestic animals. The paper also presents perspectives forfuture research regarding the possibility of discovering othersand flea species, adaptation to new hosts, and the interchangeof tungids between hosts from natural and modified habitats.

Morphology and taxonomy

Currently, the genus Tunga includes the following species:T. penetrans (L., 1758); Tunga caecata (Enderlein, 1901);Tunga caecigena Jordan & Rothschild, 1921; Tungatravassosi Pinto & Dreyfus, 1927; Tunga bondari Wagner,1932; Tunga terasma Jordan, 1937; Tunga callida Li & Chin,1957; Tunga libis Smit, 1962; Tunga monositus Barnes &Radovsky, 1969; Tunga trimamillata Pampiglione et al.,2002; Tunga bossii De Avelar et al., 2012; Tunga bonnetiBeaucournu & González-Acuña, 2012; and Tungahexalobulata De Avelar et al., 2013. Tunga penetrans is themost well-known species, having been described in the eigh-teenth century and referred to in the literature as the sand flea,sandflöh, puce de sable, chigoe, jigger, chigger, chique, nigua,and bicho-de-pé, among other names. In Peru alone, whensearching for the evidence of tungiasis in pre-HispanicAmerica, Maco et al. (2011) used 35 different local namesfor T. penetrans.

Eight of the 13 species of the genus Tunga have knownmales: T. penetrans, T. terasma, T. caecigena, T. callida,T. libis, T. monositus, T. trimamillata, and T. bonneti. Fourspecies—T. travassosi , T. bondari , T. bossii , andT. hexalobulata—are known only by their neosomes. Onlytwo species—T. penetrans and T. monositus—have immatureforms that have been described. The species T. libis,T. bondari, T. bossi, and T. hexalobulata are known onlythrough a small number of specimens.

Neosomes vary in form and size, but the enlargement of theabdomen generally occurs between abdominal segments IIand III, as seen in T. caecigena (Jordan 1962), T. monositus(Barnes and Radovsky 1969), and T. penetrans (Eisele et al.2003). The posterior part has the form of a caudal disk-like orconical prominence that bears respiratory, anal, and genitalapertures and is exposed through an opening in the host’s skin(Audy et al. 1972). In the dorsal view, the caudal disk issclerotized, resembling a crater. Data regarding the morphol-ogy of neosomes are presented in Table 1. For the first time,the neosome of T. bondari is illustrated, although a briefdescription was included in De Avelar (2010). Neosomes ofT. travassosi have been described with the head and thoraxevaginated in relation to the abdomen (Pinto and Dreyfus1927). However, after the observation of specimens depositedin the scientific collection of the Museum of Zoology of theUniversity of São Paulo, Brazil, and the Department ofParasitology of the Federal University of Minas Gerais,Brazil, it was verified that such structures are, in fact, invag-inated, and they can be seen only after dissection of theneosomes.

Figure 1 shows the shape of the gravid females of Tungaspecies found both in wild and domestic animals. Figure 1l is adorsal view of T. bonneti, whereas in the other panels, theneosomes are shown in a lateral view. Figure 2 showsneosomes after dissection from their respective hosts. Aneosome of the semisessile flea Hectopsylla pulex (Haller,1880) is included for comparison.

Geographical distribution

Species of Tunga have been found from 34° 41′N to 33° 29′S and from 38° 30′ W to 135° 30′ E. According to Barnesand Radovsky (1969), the center of distribution and theapparent origin of the genus Tunga are in the Neotropicalregion. Indeed, of the 13 described species, nine are re-stricted to South America, and another, T. penetrans, ex-hibits a wide Neotropical distribution, as it is now perma-nently established in much of tropical Africa (Lewis 1998).In spite of occasional records of Tunga fleas on humans inthe USA (Bell et al. 1979; Brothers and Heckmann 1975;Goldman 1976; Reiss 1966; Sanusi et al. 1989), Italy(Veraldi et al. 1996; Veraldi and Valsecchi 2007), and

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New Zealand (Pilgrim 1993), sand fleas do not appear tohave established themselves in these countries.

De Avelar (2010) described the presence of T. penetrans inthe following countries: Argentina, Brazil, Colombia, Chile,Ecuador, Guyana, French Guiana, Paraguay, Peru, Suriname,Trinidad, Uruguay, Venezuela, and the Caribbean Islands inLatin America and South Africa, Angola, Botswana,Cameroon, Congo, Ivory Coast, Eritrea, Gabon, Ghana,Guinea, Liberia, Libya, Madagascar, Mali, Mauritania,Mozambique, Namibia, Niger, Nigeria, Kenya, CentralAfrican Republic, São Tomé, Senegal, Sierra Leone,Somalia, Sudan, Tanzania, Tunisia, Uganda, Zaire, Zambia,Zanzibar, and Zimbabwe in Sub-Saharan Africa. According toPampiglione et al. (2009), tungiasis has been reported inapproximately 70 nations.

Except for T. penetrans, Table 2 presents the geographicaldistribution by country and respective state or province wherethe species have been recorded as well as the ranges ofdistribution and altitude. Eight of the 13 species occur inBrazil, six of which are endemic in that country. Althoughthe extent of the distribution depends upon the number oflocalities recorded for the species, and although T. bossii andT. hexalobulata have been found only in the localities inwhich they were described, the ranges of the distribution ofeach species, which vary from 494 to 5,465 km, may alsoindicate the level of dispersion of each species. Similarly,

certain species, such as T. trimamillata, T. libis, andT. bonneti, which are found in the Andean regions, can alsooccur at high altitudes. Except for new Brazilian occurrences(Table 3), all of the records of other localities of capture weredetailed and presented by Beaucournu et al. (2012b) alongwith their geographical coordinates.

Hosts

Because the degree of specificity among flea/host species isvariable, both fleas and hosts can be classified by the patternof their relationships to separate natural and casual associa-tions (Holland 1964; Krasnov 2008; Marshall 1981; Wenzelland Tipton 1966). In these circumstances, hosts can be con-sidered as true, primary, accidental, or secondary for a givenspecies of flea. True hosts, also called normal, essential, orprimary hosts, are those that provide favorable conditionsunder which a flea species can reproduce indefinitely.However, according to Holland (1964), the primary host isderived from ancient or even original associations. Accidentalhosts are those that are due purely to chance and may alsoinclude erroneous records arising from a mistaken host or fleaidentification; however, as noted by Sakaguti and Jameson(1962), some cases considered to be accidental hosts might, infact, be alternative true hosts.

Table 1 Morphology and morphometry of the neosomes of Tunga species

Tunga species Neosomes

Shape Measurements (mm)(length×width×height)

Head and thoraxin relation to theabdomen (lateral view)

Caudal disk(segments IV–X)

T. penetrans Globular without lobes 6×5×4 Evaginated Flattened, wider than long

T. caecata Globular without lobes 7×6×6 Invaginated Conical, almost as wide as long

T. travassosi Globular without lobes 13×8×10 Invaginated Conical, as wide as long

T. terasma Subcylindrical with fourlateral prominent lobes

10×9×13 Evaginated Cylindrical, longer than wide

T. bondari Mushroom-shaped with a stem,as that generated by a nuclearexplosion

6×6×5 Evaginated Cylindrical, longer than wide

T. caecigena Elliptical with four lobes: dorsal and ventralportions of similar dilatation

7–10×5×6 Not visible in profile Cylindrical, longer than wide

T. callida Spherical with four lobes: dorsal portion moreswollen than the ventral portion

4.5×4.5×4.5 Not visible in profile Cylindrical, as long as wide

T. libis Vertically elliptical and without lobes higher than long Not visible in profile –

T. monositus Bell-shaped with 8 lobes, arranged as4 large outer lobes and 4 small inner lobes

6×5.4×4.5 Evaginated but not visible in profile Flattened, wider than long

T. trimamillata Globular with 3 lobeslocated anteriorly

12×5×5 Evaginated but not visible in profile Conical, wider than long

T. bossii Globular without lobes 9×8×7 Invaginated Flattened, wider than long

T. bonneti Horizontally elliptical with rugbyball shape

10×6 Invaginated –

T. hexalobulata Spherical with six lobes located anteriorly,pearl-white colored, slightly compressedin anterior direction

4×4×4 Evaginated but not visible in profile Conical, wider than long

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A secondary host is an intermediate category for thoseconsidered neither a true nor an accidental host. According

to Holland (1964), this category is transitional for some ani-mals because a secondary host may eventually become a true

Fig. 2 Neosomes of somespecies of Tunga after removalfrom their hosts: A T. penetrans;B T. travassosi; C T. terasma; DT. bondari; E T. monositus (afterLavoipierre et al. 1979); FT. trimamillata; GT. hexalobulata

Fig. 1 Shape of gravid femalesof the species of Tunga: AT. penetrans; B T. caecata; CT. caecigena; D T. travassosi; ET. terasma; F T. bondari; GT. callida; H T. libis; IT. monositus; J T. trimamillata;KT. bossii; L T. bonneti; MT. hexalobulata

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Tab

le2

Geographicald

istributionof

speciesof

thegenusTunga

Species

Countries:statesor

provinces

Lim

itsof

distributio

nReferences

Localities

(from/to

)Extension

(km)

Altitude

(m)

T.caecata

Brazil:Minas

Gerais(M

G),Paraná

(PA),

São

Paulo

(SP)

Caratinga

MG/Curitiba

PA965

533to

1,141

Linardi

andGuimarães(2000)

T.travassosi

Brazil:SP,M

GSorocabaSP/BeloValeMG

494

566to

800

Linardi

andGuimarães(2000)

T.terasm

aBrazil:Goiás

(GO),MG,S

P,Espírito

Santo

(ES),MatoGrossodo

Sul

(MS)

Anápolis

GO/São

PauloSP

965

98to

1,141

Linardi

andGuimarães(2000);A

ntunes

etal.(2006)

T.bondari

Brazil:Bahia(BA),SP,M

GSalvadorBA/FrancaSP

1,268

0to

1,141

Hopkins

andRothschild

(1953);L

inardi

andGuimarães(2000)

T.caecigena

China:C

hekiang(CH),Fukien(FU),

Kiangsu

(KI),S

hanghai(SH

),Szechuan

(SZ),So

ochow

NishinomyiaHY/Futsing

FU

839

9to

229

Jordan

(1962);B

eaucournuetal.(2012b)

Japan:

Honshu(H

O),Osaka

(OS),H

yogo

(HY)

T.callida

China:Y

unnan(Y

U)

––

–Liand

Chin(1957)

T.lib

isEcuador:C

himborazo

(CM)

Riobamba

CM/Reserva

Nacional

Las

Chinchilas

3,418

0to

2,200

Smit(1962);B

eaucournuetal.(2012b)

Chile:C

hañaral(CA),Choapa(CH)

T.monositu

sMexico:

BajaCalifornia(BC),San

Martin

Island

(SM)

WashingtonCountyUT/San

Quintin

Bay

(BC)

841

0BarnesandRadovsky(1969);H

astriter(1997)

USA:U

tah(U

T)

T.trimam

illata

Ecuador:A

zuai(A

Z),Loja(LO),Santa

Isabel,C

atacocha,M

achala

Peru:P

iura

(PI)

Brazil:SP,M

G

Sujo

PI/FelixlândiaMG

5,465

29to

2,709

Fioravantietal.(2006);Ribeiro

etal.(2007);

Linardi

etal.(2013);Luchetti

etal.(2005a)

T.bossii

Brazil:Rio

deJaneiro(RJ)

ItatiaiaNationalP

arkRJ

–2,359

DeAvelaretal.(2012)

T.bonneti

Chile:A

tacama(AT),Santiago

(SA),

Lim

arí(LI),H

uasco(H

U),Antofagasta

(AN),ElL

oa(EL)

Quebradade

Inca

EL/Dunas

Las

CrucesSA

1,405

0to

3,794

Beaucournuetal.(2012a)

T.hexalobulata

Brazil:MG

FunilândiaMG

–692

DeAvelaretal.(2013)

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hos t . Accord ing to Marsha l l (1981) , f rom theectoparasitological viewpoint and depending upon the speciesnumber of their true hosts, fleas can be regarded as one of thefollowing: monoxenous (only one host), oligoxenous (two ormore host species in the same genus), pleioxenous (two ormore host genera in the same family), or polyxenous (severalhosts in multiple families).

Among the 13 known species of Tunga, T. penetrans is themost promiscuous, having been found on hosts belonging toeight different orders of mammals, including Cingulata,Pilosa, Artiodactyla, Perissodactyla, Carnivora, Rodentia,Primates, and Proboscidea; in total, T. penetrans has beenfound on 27 genera of wild and domestic animals (DeAvelar 2010) in addition to two occurrences that have onlyrecently been recorded (Frank et al. 2012; Widmer andAzevedo 2012). However, in spite of the broad spectrumand category of hosts, the pig is considered the most importantanimal reservoir for T. penetrans (Pampiglione et al. 1998;Ugbomoiko et al. 2008). Humans and dogs might be consid-ered secondary hosts or even true or essential hosts undergo-ing the process of adaptation. The parasitism of T. penetranson elephants (Ruthe 1961), gorillas (Ewing and Fox 1943),and monkeys (Fitzsimmons 1966) should be seen as acciden-tal. However, because the identification of this species is notalways performed by experts and is sometimes based on thesole criterion of “penetrating fleas,” some misidentificationsmay have occurred. In fact, records of T. penetrans on bats(Blanchard 1890) may be attributed to the sessile fleaH. pulex. Similarly, the infestation of this species on Gallusgallus cited by Macchiavello (1948) might have been con-fused with the stick-tight flea Echidnophaga gallinacea(Westwood, 1875), and the parasitism on the passerineVolatinia jacarina reported in Lima and Hathaway (1946), ifnot accidental, must be attributed to Hectopsylla psittaci

Frauenfeld, 1860. Similarly, the occurrence of T. bondari onCariama cristata, cited by Hopkins and Rothschild (1953), islikely an accidental finding.

Concerning domestic animals, until now, only three speciesof sand fleas have been found as ectoparasites: T. penetrans onthe pig, cow, dog, cat, and horse; T. trimamillata on the cow,goat, sheep, and pig; and T. hexalobulata, which was recentlyfound on cattle. Only T. penetrans and T. trimamillata parasitizehumans. The other 10 species exclusively infest wild animals,regardless of the number of host species. These species arelisted in Table 4 and are based on Beaucournu et al. (2012b),Cunha (1914), Hopkins and Rothschild (1953), Johnson(1957), Lima and Hathaway (1946), Linardi and Guimarães(2000), Pinto (1930), and several studies included in De Avelar(2010). Host nomenclature follows Wilson and Reeder (2005).

Another category of host is experimental animals, such asMus musculus (Lavoipierre et al. 1979) and Wistar rats (analbino strain ofRattus norvegicus), which are used to establishthe life cycle of T. penetrans in the laboratory (Feldmeier et al.2007; Nagy et al. 2007), or dogs, which are used to test theefficacy of drugs against tungiasis (Klimpel et al. 2005).

According to Smit (1962), the genus Tunga comprisestwo species groups that are separated by morphologicalcharacteristics and host affinities: caecata and penetrans.In the caecata group, which is considered the most prim-itive, the following species are currently included, all ofwhich exclusively parasitize rodents: T. caecata,T. caecigena, T. callida, T. libis, T. monositus, T. bossii,and T. bonneti. The finding of T. caecigena on Suncusmurinus (Insectivora) might be accidental. The penetransgroup is the evolutionarily advanced, as it is composed ofT. travassosi, T. bondari, T. terasma, T. trimamillata,T. hexalobulata, and obviously T. penetrans, with the firstthree species associated primarily with edentates.

Table 3 New occurrences of species of Tunga

Species of Tunga New occurrences

Localities/states References

T. caecata Caratinga/MG: 19° 47′ S/44° 52′ W, 586 mNova Lima/MG: 20° 07′ S/43° 51′ W, 817 mSão Paulo/SP: 23° 32′ S/46° 38′ W, 761 mSão João da Boa Vista/SP: 21° 58′ S/46° 48′ W, 774 m

De Avelar (2010); Linardi and Guimarães (2000);De Moraes et al. (2003)

T. travassosi Belo Vale/MG: 20° 24′ S/44° 01′ W, 800 m Linardi (unpublished)

T. terasma Alegre/ES: 20° 45′ S/41° 29′ W, 150 mPantanal da Nhecolândia: MS: 18° 59′ S/56° 39′ W, 98 m

Antunes et al. (2006); Medri (2008)

T. trimamillata Barretos/SP: 20° 33′ S/48° 34′ W, 556 mRio Novo/MG: 21° 28′ S/43° 07′ W, 416 mFelixlândia/MG: 18° 44′ S/44° 52′ W, 652 m

Vaz and Rocha (1946); Rodrigues and Daemon(unpublished work); Ribeiro et al. (2007);Linardi et al. (2013)

T. hexalobulata Funilândia/MG: 19° 22′ S/44° 03′ W, 692 m De Avelar et al. (2013)

It is important to stress that all new occurrences are recorded from Brazil.

MGMinas Gerais, SP São Paulo, ES Espírito Santo, MSMato Grosso do Sul

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However, regardless of Smit’s proposal and accordingto Traub (1980), fleas generally parasitize the hosts withwhich they evolved. Thus, primitive hosts tend to haveprimitive fleas, whereas the most advanced mammals areassociated with the most evolutionarily recent fleas. Thus,the primitive hosts of sand fleas might have been animalssuch as the Edentata, which are devoid of means toremove the neosomes (incisor teeth, nails) inserted in theinfested sites (feet, belly, skin of abdomen). It is alsoassumed that tungids and their primitive edentate hostsoccurred in Pangaea, and later, with the fragmentation ofthe continental blocks, both were isolated in SouthAmerica, with the fleas then undergoing adaptive radia-tion and infesting new hosts (Traub 1985). After thedisappearance of the primitive hosts in certain regions,such as the Nearctic and Palearctic, rodents became theprimary reservoirs (Mascarenhas 2002).

A recent study based on the molecular phylogeny offleas indicated that the basal position in the cladogram

and the association of several species of the penetransgroup with basal mammals (sloths and armadillos) sug-gest that the origin and diversification of Siphonapteracoincide with the diversification of basal mammals(Whiting et al. 2008). Possibly, mammals such as sloths(Pilosa) and armadillos (Cingulata) are the primary hosts,with other mammals (pigs, dogs, cats, rats, etc.) corre-sponding to secondary associations (Whiting et al. 2008).Wild pigs are also speculated to have been the primitivehosts, despite the meager records thus far reported.

It is known that domestic animals came to Brazil soonafter its colonization by Europeans. At that time, wildanimals such as the wild pig and the capybara hadalready been domesticated by indigenous natives. Thus,the extent to which wild and domestic pigs in the sameareas and locations might have interchanged their ecto-parasi tes is st i l l unknown. In fact , in Angola,T. penetrans was found infesting the wild suidPotamochoerus porcus (Ribeiro 1974).

Table 4 Hosts species for Tunga species

Species of Tunga Type: number of true hosts Species of mammal hosts

T. penetrans Polyxenous Artiodactyla: Bos taurus, Sus scrofa, Capra hircus, Ovis aries, Pecari tajacu, Lama glama,Vicugna vicugna, Potamochoerus porcus

Carnivora: Canis familiaris, Felis catus, Panthera oncaCingulata: Dasypus novencinctus, D. hybridus, Chaetophractus villosusPerissodactyla: Tapirus terrestris, Equus cabalus, Equus sp.Pilosa: Tamandua tetradactyla, Myrmecophaga tridactylaPrimates: Homo sapiens, Gorilla gorilla, Papio sp.Proboscidea: Loxodonta africanaRodentia: Cuniculus paca, Dasyprocta punctata, Mus musculus, M. musculoides, Rattus

rattus, Rattus norvegicus, Cavia porcellus, Cavia aperea,Myoprocta acouchy, Hystrix sp.

T. caecata Polyxenous Rodentia: M. musculus, R. rattus, R. norvegicus, Akodon cursor, Necromys pixuna,Nectomys squamipes, Oligoryzomys nigripes, Oxymycterus sp., Rhypidomys mastacalis

T. travassosi Monoxenous Cingulata: Dasypus novemcinctus

T. terasma Pleioxenous Cingulata: Cabassous unicinctus, Dasypus novemcinctus, Euphractus sexcinctus,Priodontes maximus

T. bondari Monoxenous Pilosa: Tamandua tetradactyla

T. caecigena Polyxenous Rodentia: R. rattus, R. norvegicus, M. musculus, Mus bactrianusInsectivora: Suncus murinus

T. callida Pleioxenous Rodentia: Rattus sp., R. rattus, R. norvegicus, Apodemus chevrieri, M. bactrianus,Eothenomys custos

T. libis Pleioxenous Rodentia: Akodon mollis, Phyllotis andium, Phyllotis darwini

T. monositus Pleioxenous Rodentia: Peromyscus maniculatus, P. eremicus, P. crinitus, Neotoma lepida, Neotoma sp.

T. trimamillata Polyxenous Artiodactyla: Bos taurus, Sus scrofa, Capra hircus, Ovis ariesPrimates: Homo sapiensRodentia: Hydrochoerus hydrochoerus

T. bossii Monoxenous Rodentia: Delomys dorsalis

T. bonneti Oligoxenous Rodentia: Phyllotis darwini, P. xanthopygus

T. hexalobulata Monoxenous Artiodactyla: Bos indicus

Tunga sp. (caecata group) – Rodentia: Akodon montensis, Delomys sublineatus, Oligoryzomys nigripesDidelphimorphia: Monodelphis americana

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Infestation

Flea infestations on hosts are usually defined by their meanabundance and prevalence. From an epidemiological point ofview, mean abundance and prevalence have different mean-ings. Abundance, formerly known as the rate of infestation (orinfection) or the index of parasitism (Marshall 1981), is aparameter that has been little used, mainly because the parasiteload and intensity of infestation have been considered, incor-rectly, to be synonymous by some ectoparasitologists. Meanabundance, however, is a parameter that can be employed asan indicator of the state of health of the host. Thus, highabundance might be related to the inability of the host tooppose the action of the parasite by means of its immunesystem and/or its behavior (for example, by grooming), assuggested by Stanko et al. (2002). In this respect, the effect ofthe age and sex of the host on parasite abundance requiresfurther investigation because the defensive capacity of mam-mals may well increase or decrease over time and ectoparasitegrooming might be more prevalent in one of the sexes.Multiple infestations of a single host by ectoparasites ofdifferent taxonomic groups may also influence the meanabundance of fleas, as these infestations are mediated byseveral types of ecological associations (intra- and interspe-cific competition, predation, mutualism, etc.). Furthermore, anincrease in the mean abundance of fleas might reflect theincreasing mortality of a host following infection by apathogen.

Although most adult fleas spend a part of their time inthe nest and certain species are almost exclusively nestinhabitants as adults, mammal fleas are commonly foundon their hosts’ bodies, often in considerable numbers. Inneosomatic fleas, the largest abundance recorded on asingle individual was 7,000 alakurt Dorcadia from a sheep(Ioff 1950 in Marshall 1981). In tungids, 31 T. caecigenawere counted on a Rattus species (Jordan 1962). InT. travassosi, tens of neosomes can be found in the bellyof its host, Dasypus novemcinctus. Regarding T. penetrans,approximately 80 lesions were found on dogs, 50 on cats,16 on rats, and 199 on humans from Fortaleza, Brazil(Heukelbach et al. 2004a), whereas in a community in ruralNigeria, Ugbomoiko et al. (2008) observed the followingmaximum numbers of lesions: 184 on pigs, 21 on dogs,and 13 on Rattus rattus. In a study of flea infestations ofPanthera onca, Widmer and Azevedo (2012) recordedmore than 20 lesions on a young female.

Prevalence is also related to the propagation of ectopar-asites on their respective hosts. Thus, a high prevalencemight be the result of a microenvironmental overlap amonghosts that, when associated with environmental factors,would favor the development of immature stages. In thiscontext, prevalence would be related to spatial factors,including the territoriality and dispersion of the host.

Given the vectorial capacity of fleas, prevalence potential-ly represents a tool with which to measure the dissemina-tion of pathogens.

Infestations vary according to host age, sex, size, behavior,host mobility, habitat, and climate (Marshall 1981). The pref-erence for host females can be related to hormonal cycles, asobserved between Spilopsyllus cuniculi and Oryctolaguscuniculus and between Cediopsylla simplex and Sylvilagusspp. Preferences for male hosts, as observed in rats, may existbecause males have larger home ranges, are generally largerthan females, and exhibit territorial behavior. Other sex andage preferences result from grooming because males are moreefficient groomers than females and adults groom more thanyoung individuals. Regarding environmental factors, Linardiand Krasnov (2013) observed that in three hosts (Monodelphisdomestica, Necromys lasiurus, and Oligoryzomys eliurus)collected at different localities across Brazil, the mean fleaabundance significantly increased with an increase in themean annual air temperature and the proximity to the equator.For both M. domestica and N. lasiurus, abundance also de-creased with altitude.

However, interpretations based on comparisons of theseparameters should be made with caution when consideringdata from different regions that were not obtained in the sameperiod. Moreover, the mode of capture, i.e., the number oftrappings/unit time, is rarely described and varies amongdifferent studies; the baits used are not always the mostsuitable and can vary in both quality and quantity; hosts maybelong to different taxonomic groups with different habits andhabitats; and the sites of parasitism are not always the same ondifferent hosts. Perhaps the most important factor in quantify-ing parameters, however, relates to the timing of fleas leavingthe host. Fleas leave those hosts that have been confined intraps the longest and abandon the carcass completely afterdeath (Marshall 1981; Pollitzer 1954). Consequently, moreaccurate data would be obtained as soon as possible aftercapture and, if possible, while still in the field. However, thissituation does not apply to sand fleas in which gravid femalesremain attached to the hosts even after their death.

In spite of these variables, some available figures for prev-alence on certain hosts at different locations and times areshown separately for T. penetrans (Table 5) and other sandfleas (Table 6). As shown in Table 5, with the exception of thedata from Rodrigues et al. (2008), the prevalence of tungiasisin stray dogs is similar in poor communities and shanty towns:45.5 to 60.9 %.

Considering that the bovine tungiasis previously attributedto T. penetrans in Barretos, São Paulo State, Brazil (Vaz andRocha 1946), and Felixlandia, Minas Gerais State, Brazil(Ribeiro et al. 2007), was in fact caused by T. trimamillata(Linardi et al. 2013), it is likely that records pertaining to Jataí,Goiás State (Da Silva et al. 2001), and Santa Fé do Sul, SãoPaulo State (Moraes et al. 1992), are also of T. trimamillata.

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Sites of Attachment

Tungid fleas show consistent preferences for attachmentsites. The semipenetrating flea H. pulex prefers bats’heads, especially body regions with sparse hairs, such as

the ears (Esbérard 2001), although these fleas are alsofound on the tragus, shoulder blade and tibia, anus, wings,axilla, mouth, and dactylopatagium (Luz et al. 2009). Onpangolins, the pulicid N. euloidea is usually attached tothe soft skin of the ventral region.

Table 5 Prevalence of infestation by T. penetrans on hosts in different locations

Location, state, country Hosts References

Species Examined (no.) Infested (no.) Prevalence (%)

Coqueiros do Sul, RS, Brazil Pigs 72 64 88.9 Pedroso-de-Paiva et al. (1997)

São Tomé Island, Africa 100 28 28.0 Pampiglione et al. (1998)

Araruama, RJ, Brazil 12 2 16.6 Carvalho et al. (2003)

Rural zone, Nigeria 31 17 54.8 Ugbomoiko et al. (2008)

Curitiba, PR, Brazil Dogs 7.811 58 0.7 Vernalha et al. (1984)

Araruama, RJ, Brazil 123 75 60.9 Carvalho et al. (2003)

Fortaleza, CE, Brazil 150 76 50.7 Heukelbach et al. (2004a)

Rural zone, Nigeria 11 5 45.5 Ugbomoiko et al. (2008)

Juiz de Fora, MG, Brazil 101 2 2.0 Rodrigues et al. (2008)

Manaus, AM, Brazil 42 20 47.6 Corrêa et al. (2012)

Araruama, RJ, Brazil Cats 24 2 8.3 Carvalho et al. (2003)

Fortaleza, CE, Brazil 158 72 45.6 Heukelbach et al. (2004a)

Fortaleza, CE, Brazil Rats 34 14 41.2 Heukelbach et al. (2004a)

Rural zone, Nigeria R. rattus 17 5 29.4 Ugbomoiko et al. (2008)

Rural zone, Nigeria M. minutoides 13 2 15.4 Ugbomoiko et al. (2008)

Buenos Aires, BA, Argentina C. villosus 4 1 25.0 Ezquiaga et al. (2008)

Buenos Aires, BA, Argentina D. hybridus 13 1 7.7 Ezquiaga et al. (2008)

Uberlândia, MG, Brazil M. tridactyla 3 2 66.7 Frank et al. (2012)

Pantanal region, MS, Brazil P. onca 12 12 100 Widmer and Azevedo (2012)

Table 6 Prevalence of infestation by some sand fleas on the respective hosts

Tunga species Hosts Location References

Species Collected(no.)

Infested(no.)

Prevalence(%)

T. caecata R. norvegicus 824 82 9.9 São Paulo, SP, Brazil Meira (1934)R. rattus 445 13 2.9

M. musculus 135 2 1.5

T. caecigena R. rattus 250 68 27.2 Soochow, China Wu (1930) in Jordan (1962)R. norvegicus

T. terasma D. novemcinctus 34 4 11.7 Alegre, ES, Brazil Antunes et al. (2006)

E. sexcinctus 31 1 3.2 Pantanal da Nhecolândia, MS, Brazil Medri (2008)

T. monositus P. eremicus

P. crinitis 21 6 28.6 Washington County, UT, USA Hastriter (1997)

N. lepida

T. trimamillata Bos taurus 170 130 76.4 Felixlândia, MG, Brazil Ribeiro et al. (2007)

T. trimamillata or T. penetrans Bos taurus 550 375 68.2 Jataí, GO, Brazil Da Silva et al. (2001)

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Among sand fleas, T. penetrans occurs commonly betweenthe toes and periungueal regions when parasitizing humans(Eisele et al. 2003), justifying the vernacular name bicho-de-pé in Brazil (Cunha 1914; Linardi and Guimarães 2000). Thisspecies also can be found on other sites, such as the hands,soles, elbows, neck, anus, gluteal area, genital region, but-tocks, heels, groin, face, etc. (Bezerra 1994; Heukelbach et al.2002). Some authors (Cardoso 1981; Clyti et al. 2003) havealso reportedmultiple sites spread over a large part of the bodyon a single person.

On pigs, T. penetrans occurs particularly on the feet, snout,and scrotum (Cooper 1976) but also on the mammary glands(Pedroso-de-Paiva et al. 1997) and in the calcaneal region(Pampiglione et al. 2009). On both dogs and cats, neosomescan be seen around the claws, on the pads and, especially, onthe muzzle (Heukelbach et al. 2004a). Female dogs can alsoexhibit lesions in the nipples (Klimpel et al. 2005). OnBrazilian wild mammals, Frank et al. (2012) reported lesionson the feet of the giant anteaterMyrmecophaga tridactyla, andon the jaguar (P. onca), Widmer and Azevedo (2012) ob-served neosomes confined to the animals’ paws.

When infesting bovines, goats, and sheep, neosomes of thespecies T. trimamillata are found along the coronary band, inthe coronary and digital cushions, and sometimes on the soleof the hoof (Pampiglione et al. 2009). In cattle, this species canalso be observed on the edge of the nail wall development, thatis, at the level of the perioptic tafe, as well as on the perianalarea, on the udder of cows and prepuce of bulls (Vaz andRocha 1946). On pigs, neosomes of this species also tend tobe localized on the calcaneal region and scrotum in males andthe udder in females (Pampiglione et al. 2009).

Other species of Tunga exhibit the following preferentialattachment sites on their respective hosts: T. caecata, uppersurface of rat ears (Jordan 1962); T. travassosi, dermis of theventral abdominal region of edentates (Lima 1943; Pinto1930); T. terasma, ventral abdomen and toes of edentates(Antunes et al. 2006); T. bondari, ventral abdomen of eden-tates (Wagner 1932); T. caecigena, at the edge of the pinna butalso on the dorsal surface of rat ears and, in one case (only on aspecimen of R. rattus), at the base of the tail (Jordan 1962;Yang 1955); T. callida, rear end of the body, especially aroundthe anus of rats (Li and Chin 1957); T. libis, ears of rodents(Beaucournu et al. 2012a); T. monositus, basal portion of theupper surface of the pinna of rodents (Barnes and Radovsky1969); T. bossii, base of the tail of wild rodents (De Avelaret al. 2012); T. bonneti, parallel to the great axis of the tail ofrodents (Beaucournu et al. 2012a); and T. hexalobulata, cor-onary band of cattle (De Avelar et al. 2013). Figure 3 showssites of attachment for neosomes of some tungids on theirhosts, including H. pulex.

Considering the data recorded thus far, the most frequentattachment sites are the feet, ventral abdominal, ears, and tailsof hosts. The choice of these respective sites depends upon the

following factors: (i) regions that regularly contact the soil,such as the feet in humans and domestic and wild animals orthe ventral abdominal region in both domestic and wild mam-mals; (ii) areas from which the hosts have the greatest diffi-culty dislodging the parasites by grooming or eating, such asthe ears and tail in rats or the ventral abdominal region inedentates, which are devoid of incisor teeth and nails; and (iii)the structure of the hair and thickness of the coat related tomicroclimates such as temperature and skin structure, as inbats and pangolins (Marshall 1981). According to Nagy et al.(2007), older cats and dogs have fewer neosomes than youngindividuals because of the thicker skin on their paws. Becausespecies of Tunga have a reduced pleural arch (Traub 1972)and, consequently, are unable to jump very high, the lesionsproduced by T. penetrans are more concentrated or confinedto the feet of animals, as reported by Klimpel et al. (2005).

Impact on the hosts

The impact of tungid fleas depends on the sites of attachmenton their hosts. The effects of parasitism are well known forT. penetrans, as it is the best known and disseminated speciesin the genus, infesting humans and domestic and wild animals.

In humans, the symptoms, direct impact, and complicationshave been well documented. Briefly, intense pain and itchingare perceived to be the most irritating symptoms (Feldemeieret al. 2004), with most infestations occurring on the feet andprovoking deformation of the digits and the loss of toenails. Insome cases, severe inflammation and deep skin fissures pre-vent individuals from walking normally (Ariza et al. 2007;Heukelbach et al. 2007; Hoeppli 1963; Matias 1989). In theKasulu district, western Tanzania, Mazigo et al. (2012) ob-served the following symptoms in individuals examined fortungiasis: itching (68.3 %), pain (38.6 %), ulcers (30.1 %),difficulty walking (22.1 %), and loss of toenails (21.3 %).

Superinfected lesions, primarily caused by Staphylococcusaureus and Gram-negative bacteria, lead to the formation ofpustules, suppuration, and ulcers that may also be a port ofentry forClostridium tetani (Greco et al. 2001; Obengui 1989;Soria and Capri 1953; Tonge 1989). Other pathogenic micro-organisms isolated from superinfected lesions includeStreptococcus pyogenes, Enterobacteriaceae, Bacillus spp.,Enterococcus faecalis, Pseudomonas spp., and various otheranaerobic bacteria (Feldmeier et al. 2002; Heukelbach et al.2007). Symptoms and signs used to determine the severity ofacute tungiasis have been reported by Kehr et al. (2007).

Other complications include cases of gangrene,lymphangitis, lymphadenitis, and sepsis (Veraldi andSchianchi 1999). Brumpt (1949) reported a strain ofYersinia pestis isolated from T. penetrans in the Congo.Using molecular techniques, Wolbachia was also identifiedin a neosomic female T. penetrans from Ghana (Fischer

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et al. 2002), Brazil (Heukelbach et al. 2004b) as well as inswine from localities in Ecuador and in humans fromdifferent localities in Burundi, Kenya, and Zaire (Luchettiet al. 2004; 2005b).

Despite the effects of tungiasis in humans, very little isknown of its parasitism on animals, especially wild mammals.In pigs, the infestation causes walking difficulties due to thepresence of the parasite in the hoofs. When the lesions arelocated in the teats, they can cause agalactia and mastitis inlactating sows due to obstruction of the galactophorous chan-nel, blocking milk production and subsequent involution ofthe mammary glands and causing starvation of the piglets(Pedroso-de-Paiva et al. 1997; Verhulst 1976).

Infested dogs change their position constantly, lick theirpads, and are reluctant to stand up (Heukelbach et al. 2004a).In severe cases, dogs are unable to walk and may even die(Wolffhügel 1910), presumably due to the superinfection oflesions, leading to septicemia. Loss of digits can also beobserved in rat tungiasis with severe inflammation(Heukelbach et al. 2004a).

Infestation on the feet of giant anteaters provokes inflam-mation that prevents the animals from breaking up termitariawith their forefeet, thus preventing them from accessing their

main food. According to Frank et al. (2012), tungiasis mostlikely prevents or at least hinders this natural behavior, and asa consequence, the anteaters avoid common food sources inpreference for those that are less suitable but more accessible.

T. trimamillata is the second species for which the effects onits hosts are known. In humans, local inhabitants of the Andeanregions that have been co-infested by T. penetrans andT. trimamillata report that the infestation caused by the latteris more painful (Pampiglione et al. 2009). In bovines, infesta-tion causes deformation of the nails. Some animals becomecompletely crippled, refusing to walk or even unable to stand.When such injuries occur in a breeding animal, its inability tosustain its own weight can be compounded by pregnancy. Theprocess is often complicated by secondary infection with ulcer-ation on the upper edge of the nails as a consequence of therupture of the neosomes caused by excoriation. In some cases,flies deposit their eggs in the ulcers that are so formed, increas-ing the destruction of the living tissue (Vaz and Rocha 1946).Wolbachia was also found in samples of T. trimamillata col-lected from goats and cattle in Santa Isabel, Ecuador, andidentified through PCR amplification and sequencing of thebacterial ribosomal 16S and ftsZ genes, with prevalences of 40and 11 %, respectively (Luchetti et al. 2004, 2005b).

Fig. 3 Sites of attachment ofsome neosomes on their hosts: AH. pulex on the bat’s headMolossus sp. (courtesy of JúliaLins Luz); B T. caecata on the earof Oryzomys nigripes; C T. libison the ear of Phyllotis darwini(after Beaucournu et al. 2012a);DT. bossii on the tail of Delomysdorsalis; E T. bonneti on the tailof P. darwini (after Beaucournuet al. 2012a); F T. trimamillata onthe hoof of Holstein-Zebu cow(courtesy of Elias Jorge FacuryFilho)

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Little is known about the impact of other species of Tungaon wild animals. In contrast to T. penetrans, in which bothmales and females are blood feeding (Geigy and Herbig 1949;Witt et al. 2004), the larvae and adult males of T. monositus donot feed (Lavoipierre et al. 1979). According to these authors,after becoming attached to rodent skin, adult females ofT. monositus feed principally off of fluid exudate and, for afew days, off of neutrophils, fibroblasts, collagen, and macro-phages. Blood feeding commences from the 14th day.

Neosomes of sand fleas can reach a diameter of 1 cm ormore (Table 1). T. penetrans may remain attached to the hostfor a period of more than 5 weeks (Eisele et al. 2003), whereasT. monositus lies embedded in the skin of the ear pinna for 2 or3 months (Lavoipierre et al. 1979). As in otherectoparasitoses, the lesions may affect weight gain and milkproduction, and as in humans and domestic animals, thelesions might also become infected and be a port of entry forvarious pathogens. Considering the abundance of neosomes,their attachment sites and affected organs, as well as thelifespan of the embedded sand fleas, what is the real impactof these infestations on wild animals? Armadillos are insecti-vores that use the toes of the forefeet for digging into galleriesto feed chiefly on ants, termites, and other small invertebrates.They have also been observed to roll about on ant hills todislodge and consume the resident ants. How do we evaluatethe action of tens of neosomes of T. travassosi on the toes orthe 30 cm ventral surface of armadillos? Or similarly, morethan 30 neosomes of T. caecigena over the ears or the tail of arat that measure, respectively, 24 and 180 mm? It is importantto stress that in rats, the pinna can be rotated to catch theslightest sound from almost any direction. This ability isuseful for an animal whose activity is primarily confined todarkness. Rats also control their body temperature throughtheir tails by dilating or constricting their tail blood vessels anduse their tails for balance (Yulong et al. 1995). In the samemanner, to what extent will the presence of neosomes ofH. pulex on the ears of bats inhibit their ability to navigate,considering that the ears act as biosonar-receiving antennas?

Perspectives

Among the 13 species currently included in the genus Tunga,more than 30 % have been described in the last 12 years; thus,the chances of discovering new species are high. Some sam-ples of T. penetrans have displayed slight variations whencollected from different hosts in Fortaleza, Brazil, which mayindicate the existence of different strains or races or thebeginning of such a formation (Nagy et al. 2007). Recently,De Avelar and Linardi (2010) showed that the multiple dis-placement amplification (MDA) technique enables the ampli-fication of the genomic DNA of siphonapterids that have beenpreserved for long periods, with the successful amplification

of one neosome of T. bondari that was collected in 1909. Thistechnique may be a valuable tool for molecular studies in-volving samples of sand fleas that are preserved in scientificcollections.

The Neotropical region stands out as the most promisingregion in which new taxa might be found, as it contains adiversity of biomes and at least 40 dispersion centers, 13 ofwhich are located in Brazil (Müller 1972). Furthermore, Brazilis considered a hotspot of global biodiversity (Mittermeieret al. 1998; Myers et al. 2000), as it occupies a vast area andcontains approximately 13 % of the world’s mammal fauna(Reis et al. 2006) that are recognized as valid species (Wilsonand Reeder 2005). Rodents, representing approximately 36 %of the Brazilian mammals, deserve particular attention be-cause in this country, rodents host five different Tunga speciesthat are included in the caecata group. Additionally, consid-ering that three species of Tunga that belong to the penetransgroup are primarily associated with edentates (Hopkins andRothschild 1953; Lima and Hathaway 1946; Linardi andGuimarães 2000) and that only seven of the 14 species ofBrazilian Myrmecophagidae (Pilosa) and Dasypodidae(Cingulata) (Reis et al. 2006) have been recorded as hostsfor these sand fleas, both armadillos and anteaters are taxa thatshould be further examined for occurrences of tungids be-cause they exhibit a large geographical distribution and rangethroughout various biomes (Da Fonseca et al. 1996), which,according to Krasnov et al. (2003), are among the mostpromising factors for the discovery of a new species of flea.In fact, a new species of Tunga and located in the carapace ofZaedyus pichiy and perforating the osteoderms is being nowdescribed by Ezquiaga et al. (unpublished work) fromArgentina. Additionally, it is important to verify whether, infact, Artiodactyla species represent true hosts for Tunga spe-cies because Rodrigues and Daemon (unpublished work) alsofound T. trimamillata on the capybara H. hydrochaeris inBrazil. In contrast, thus far, only M. americana of the 54Brazilian species of Didelphimorphia (Reis et al. 2006) hasbeen found to be infested with neosomes (Bossi 2003).

However, in spite of these possibilities, certain chal-lenges exist for obtaining neosomes: (i) the extraction ofthe ectoparasites of mammals without killing the host instudies that do not allow the death of the host; (ii) incom-plete inspection of the entire body of the animal by thecollector, with the primary sites of attachment such as thebelly, paws, ears, and tails not being examined; (iii) mis-diagnosis, with the lesions being confused with larvae ofCuterebra, cicatrization of animals’ bites (Beaucournuet al. 2012b) or abscesses, mycosis, larva migrans, andother symptoms; and (iv) misidentifications with otherspecies of Tunga because the taxonomic identificationsare not always performed by experts. In fact, some occur-rences attributed to T. penetrans on certain hosts are likelyincorrect (Linardi et al. 2013).

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In fleas, only adults are ectoparasitic, whereas the immaturestages develop in the soil, inside or close to the nests of therespective hosts and, consequently, are susceptible to preda-tion or environmental modifications. The prevalence andmean abundance of these ectoparasites could thus assist natureconservation studies because they can serve as indicators ofeventual alterations when compared temporally in a singlelocality. For T. penetrans, the natural habitat is primarily thesandy and warm soil of deserts and beaches (Veraldi andSchianchi 1999), thus justifying the vernacular names sandflea, sandflöh, and puce de sable, as cited by Beaucournu et al.(2012b) and Cunha (1914). Granular soils, which are consid-ered favorable for T. penetrans by the majority of authors, arealso favorable for other congeneric species (Beaucournu et al.2012a). However, both adults and immature young of otherspecies of Tunga must be searched for in the nests and bur-rows of their respective hosts, especially those of edentatesand rodents. On tropical beaches, the dispersion ofT. penetrans is ensured by infested dogs. Additionally, horsemanure used to fertilize soils aids in sand flea disseminationbecause both T. penetrans and T. trimamillata also live instables and stock farms as well as in the soil and dust closeto farms. Other fecal matter such as bat guano supports thedevelopment of H. pulex (Hastriter and Méndez 2000; Tiptonand Méndez 1966).

It seems that the soil temperature, air temperature, and airhumidity do not markedly affect the presence of T. penetransin soil samples, as observed by Linardi et al. (2010) in threegeographical regions of Brazil: Fortaleza (Ceará State), Barrado Garças (Mato Grosso State), and Alto Alegre (RoraimaState). Larvae of this species were found in the sand in a depthof 2–5 cm (Nagy et al. 2007). Certain species are univoltine,as they are collected only during one season, includingT. caecigena during the cold season and T. callida duringwinter months in China (Jordan 1962); T. monositus in Utahfrom October through April (Hastriter 1997); T. libis in June(Smit 1962), October, and November in Chile (Smit 1968);T. bonneti from July to December in Chile (Beaucournu et al.2012a); and T. hexalobulata during the dry-cool season fromApril to September in Brazil (De Avelar et al. 2013). Similarly,both T. penetrans and T. trimamillata develop better in the dryseason (Pampiglione et al. 2009), thus confirming the findingsof Hoeppli (1963), who reported for T. penetrans in Africathat “the number of sandfleas greatly decreases during therainy season.” With respect to the species of Tunga found onedentates, data included as material deposited in theRothschild collection of fleas of the British Museum(Hopkins and Rothschild 1953) indicate November as themonth in which T. travassosi, T. terasma, and T. bondariwerecollected, which corresponds to the rainy season in Brazil. ForT. caecata, Meira (1934) observed neosomes on a rat’s ear inthe months of December, February, and April, with only thelatter included in the dry-cool season in São Paulo, Brazil.

Concerning other geographical factors, only the latitude,with respect to its influence on temperature, would play a rolein distribution because the same species can be collected atdifferent altitudes (Beaucournu et al. 2012a). In Chile,T. bonneti occurs more frequently from July to December,decreasing in January and February (Beaucournu et al.2012a).

Although the treatment and prophylaxis of tungiasis are notwithin the scope of this review, it is interesting to note thatthese actions have only been performed in humans and do-mestic animals when parasitized. Treatment consists of localexcision or sterile curettage. Parasitized dogs can be treatedwith a subcutaneous application of ivermectin and healingointments and repellent (Corrêa et al. 2012).

In humans, prophylactic measures include the wearing ofshoes, improving hygiene, use of gloves for handling manure,sweeping floors, and the restriction of free movement ofpeople and infested animals among households. AccordingtoMatias (1989), in somemunicipalities of Rio Grande do SulState, Brazil, trucks carrying sand and sheaves of grass usedfor construction of houses can also act in the dissemination ofthis species.

Tetanus vaccination is recommended to prevent secondaryinfection. Both within and around the residences in two mu-nicipalities of Rio Grande do Sul State, Brazil, the pyrethroidscypermethrin and deltamethrin were used as a measure ofenvironmental control (Matias 1991). Given the diversity ofhabitats, Linardi (1998) claimed that integrated actions wererequired for the control of tungiasis, involving clinicians,veterinarians, biologists, public health specialists, and techni-cians and companies responsible for vector control. An over-view of human tungiasis and including risk factors, treatment,repellents, prevention, control, and healthcare stakeholdershas been presented by Karunamoorthi (2013).

Until recently, tungiasis provoked by T. penetrans had beenreported in approximately 70 nations, especially in LatinAmerica and Sub-Saharan Africa, most commonly affectingpoor populations (Pampiglione et al. 2009). The number ofcases has been increasing, as reported in several publicationsworldwide. Now, tungiasis is endemic or potentially endemicto 89 countries with varying degrees of incidence and preva-lence, which vary in relation to the area and population stud-ied. It has been estimated that the prevalence of tungiasis mayreach more than 50 % of the population in some of thehyperendemic zones, with often recurrent and sometimesmassive parasitic infestations that are responsible for superin-fections (Karunamoorthi 2013).

In Brazil alone, more than 106 individuals are at risk forsevere tungiasis (Heukelbach et al. 2001). In the villages ofTanzania, jigger parasitization is locally referred as inzyogo,which means “the disease of the dirty people” (Mazigo et al.2012). The treatment involves surgical extraction of the sandflea under sterile conditions, but due to the low socioeconomic

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status of some villages in Tanzania and Kenya, pins and otherunsterilized equipment are being shared for jigger removal,leading to the possible further spread of HIV and AIDS andother diseases and increased opportunity for bacterial infec-tion through the new open wounds that are often left uncov-ered (Wachira 2012).

In recent decades, ecotourism in forest areas, caves, andmountains has become another cause of the increase in thechances of human infestation by sand fleas, which usuallyparasitize other animals. Additionally, as a result of the ex-pansion of urban areas into wild environments, the opportu-nities for contact between domestic and wild animals haveincreased, thus facilitating the exchange of ectoparasites. Forthis reason, it is possible that sand fleas parasitizing wildmammals may be found on domestic mammals and viceversa. In fact, this situation may be the case for T. penetransand T. trimamillata, as pasturelands for cattle are now found incerrado areas occupied by rodents and edentates.

Acknowledgments The authors wish to thank the Conselho Nacionalde Desenvolvimento Científico e Tecnológico (CNPq) for the researchfellowship granted to P.M.L. Some data of this research constituted part ofthe PhD thesis of D.M.A in Parasitology/Post-graduate program inParasitology/Instituto de Ciências Biológicas/Universidade Federal deMinas Gerais/UFMG, Brazil. The authors would also thank the follow-ing: the Entomological Society of America for the permission in thereproduction of figures of the neosomes of T. monositus, T. bossii, andT. hexalobulata published in the Journal of Medical Entomology; theEDP Sciences also for the permission to reuse figures of neosomes ofT. libis and T. bonneti published in Parasite; and to Júlia Lins Luz andElias Jorge Facury Filho for some photos of neosomes.

Open Access This article is distributed under the terms of the CreativeCommons Attribution License which permits any use, distribution, andreproduction in any medium, provided the original author(s) and thesource are credited.

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